Co-overexpression of SWEET sucrose transporters modulates sucrose synthesis and defence responses to enhance immunity against bacterial blight in rice

Enhancing carbohydrate export from source to sink tissues is considered to be a realistic approach for improving photosynthetic efficiency and crop yield. The rice sucrose transporters OsSUT1, OsSWEET11a and OsSWEET14 contribute to sucrose phloem loading and seed filling. Crucially, Xanthomonas oryzae pv. oryzae (Xoo) infection in rice enhances the expression of OsSWEET11a and OsSWEET14 genes, and causes leaf blight. Here we show that co-overexpression of OsSUT1, OsSWEET11a and OsSWEET14 in rice reduced sucrose synthesis and transport leading to lower growth and yield but reduced susceptibility to Xoo relative to controls. The immunity-related hypersensitive response (HR) was enhanced in the transformed lines as indicated by the increased expression of defence genes, higher salicylic acid content and presence of HR lesions on the leaves. The results suggest that the increased expression of OsSWEET11a and OsSWEET14 in rice is perceived as a pathogen (Xoo) attack that triggers HR and results in constitutive activation of plant defences that are related to the signalling pathways of pathogen starvation. These findings provide a mechanistic basis for the trade-off between plant growth and immunity because decreased susceptibility against Xoo compromised plant growth and yield. The study reported in this manuscript concerns the emerging topic of the roles played by SWEET sugar transporters in plant immunity. The data reported in this manuscript show that overexpression of Clade III SWEET sucrose transporters OsSWEET11a and OsSWEET14 that are exploited by bacterial blight pathogen Xanthomonas oryzae pv. oryzae to acquire sugars for its propagation elicits immune responses and activates plant defence responses leading to enhanced resistance against bacterial as well as fungal pathogens. The findings obtained by the overexpression of OsSWEET11a and OsSWEET14 in rice show that sucrose transport occurs via an apoplastic route, and overexpression of these sugar transporters inhibits sucrose synthesis and transport, which explains the inverse relationships between plant growth and yield, and resistance to pathogens. Moreover, our results show that sucrose transport and pathogen responses are coupled processes, and provide evidence for the concept that pathogen-induced starvation is linked to plant defence.Also, to the best of our knowledge this is the first study where we show that disease susceptibility genes OsSWEET11a and OsSWEET14 can lead to hypersensitive reaction leading to enhanced plant immunity.